Clinical Features of Gastric Signet Ring Cell Cancer: Results from a Systematic Review and Meta-Analysis

Mariagiulia Dal Cero; Maria Bencivenga; Drolaiz H.W. Liu; Michele Sacco; Mariella Alloggio; Kelly G.P. Kerckhoffs; Federica Filippini; Luca Saragoni; Mar Iglesias; Anna Tomezzoli; Fátima Carneiro; Heike I. Grabsch; Giuseppe Verlato; Lorena Torroni; Guillaume Piessen; Manuel Pera; Giovanni de Manzoni

doi:10.3390/cancers15215191

Clinical Features of Gastric Signet Ring Cell Cancer: Results from a Systematic Review and Meta-Analysis

Mariagiulia Dal Cero, Maria Bencivenga^*, Drolaiz H.W. Liu, Michele Sacco, Mariella Alloggio, Kelly G.P. Kerckhoffs, Federica Filippini, Luca Saragoni, Mar Iglesias, Anna Tomezzoli, Fátima Carneiro, Heike I. Grabsch, Giuseppe Verlato, Lorena Torroni, Guillaume Piessen, Manuel Pera, Giovanni de Manzoni

^*Corresponding author for this work

Research output: Contribution to journal › (Systematic) Review article › peer-review

Abstract

Background: Conflicting results about the prognostic relevance of signet ring cell histology in gastric cancer have been reported. We aimed to perform a meta-analysis focusing on the clinicopathological features and prognosis of this subgroup of cancer compared with other histologies. Methods: A systematic literature search in the PubMed database was conducted, including all publications up to 1 October 2021. A meta-analysis comparing the results of the studies was performed. Results: A total of 2062 studies referring to gastric cancer with signet ring cell histology were identified, of which 262 studies reported on its relationship with clinical information. Of these, 74 were suitable to be included in the meta-analysis. A slightly lower risk of developing nodal metastases in signet ring cell tumours compared to other histotypes was found (especially to undifferentiated/poorly differentiated/mucinous and mixed histotypes); the lower risk was more evident in early and slightly increased in advanced gastric cancer. Survival tended to be better in early stage signet ring cell cancer compared to other histotypes; no differences were shown in advanced stages, and survival was poorer in metastatic patients. In the subgroup analysis, survival in signet ring cell cancer was slightly worse compared to non-signet ring cell cancer and differentiated/well-to-moderately differentiated adenocarcinoma. Conclusions: Most of the conflicting results in signet ring cell gastric cancer literature could be derived from the lack of standardisation in their classification and the comparison with the different subtypes of gastric cancer. There is a critical need to strive for a standardised classification system for gastric cancer, fostering clarity and coherence in the forthcoming research and clinical applications.

Original language	English
Article number	5191
Number of pages	22
Journal	Cancers
Volume	15
Issue number	21
DOIs	https://doi.org/10.3390/cancers15215191
Publication status	Published - 1 Nov 2023

Keywords

gastric cancer
pathological classification
poorly cohesive
signet ring cells
survival

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10.3390/cancers15215191Licence: CC BY

Cite this

Dal Cero, M., Bencivenga, M., Liu, D. H. W., Sacco, M., Alloggio, M., Kerckhoffs, K. G. P., Filippini, F., Saragoni, L., Iglesias, M., Tomezzoli, A., Carneiro, F., Grabsch, H. I., Verlato, G., Torroni, L., Piessen, G., Pera, M., & de Manzoni, G. (2023). Clinical Features of Gastric Signet Ring Cell Cancer: Results from a Systematic Review and Meta-Analysis. Cancers, 15(21), Article 5191. https://doi.org/10.3390/cancers15215191

@article{329de2ca93f24bc49dacdc6cc3494ff1,

title = "Clinical Features of Gastric Signet Ring Cell Cancer: Results from a Systematic Review and Meta-Analysis",

abstract = "Background: Conflicting results about the prognostic relevance of signet ring cell histology in gastric cancer have been reported. We aimed to perform a meta-analysis focusing on the clinicopathological features and prognosis of this subgroup of cancer compared with other histologies. Methods: A systematic literature search in the PubMed database was conducted, including all publications up to 1 October 2021. A meta-analysis comparing the results of the studies was performed. Results: A total of 2062 studies referring to gastric cancer with signet ring cell histology were identified, of which 262 studies reported on its relationship with clinical information. Of these, 74 were suitable to be included in the meta-analysis. A slightly lower risk of developing nodal metastases in signet ring cell tumours compared to other histotypes was found (especially to undifferentiated/poorly differentiated/mucinous and mixed histotypes); the lower risk was more evident in early and slightly increased in advanced gastric cancer. Survival tended to be better in early stage signet ring cell cancer compared to other histotypes; no differences were shown in advanced stages, and survival was poorer in metastatic patients. In the subgroup analysis, survival in signet ring cell cancer was slightly worse compared to non-signet ring cell cancer and differentiated/well-to-moderately differentiated adenocarcinoma. Conclusions: Most of the conflicting results in signet ring cell gastric cancer literature could be derived from the lack of standardisation in their classification and the comparison with the different subtypes of gastric cancer. There is a critical need to strive for a standardised classification system for gastric cancer, fostering clarity and coherence in the forthcoming research and clinical applications.",

keywords = "gastric cancer, pathological classification, poorly cohesive, signet ring cells, survival",

author = "{Dal Cero}, Mariagiulia and Maria Bencivenga and Liu, {Drolaiz H.W.} and Michele Sacco and Mariella Alloggio and Kerckhoffs, {Kelly G.P.} and Federica Filippini and Luca Saragoni and Mar Iglesias and Anna Tomezzoli and F{\'a}tima Carneiro and Grabsch, {Heike I.} and Giuseppe Verlato and Lorena Torroni and Guillaume Piessen and Manuel Pera and {de Manzoni}, Giovanni",

note = "Funding Information: This work would not have been possible without the financial support of the “Fondazione Gianesini” and the “Ricerchiamo ONLUS”. H.I.G. is supported in part by the National Institute for Health and Care Research (NIHR) Leeds Biomedical Research Centre. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care. Publisher Copyright: {\textcopyright} 2023 by the authors.",

year = "2023",

month = nov,

day = "1",

doi = "10.3390/cancers15215191",

language = "English",

volume = "15",

journal = "Cancers",

issn = "2072-6694",

publisher = "Multidisciplinary Digital Publishing Institute (MDPI)",

number = "21",

}

Dal Cero, M, Bencivenga, M, Liu, DHW, Sacco, M, Alloggio, M, Kerckhoffs, KGP, Filippini, F, Saragoni, L, Iglesias, M, Tomezzoli, A, Carneiro, F, Grabsch, HI, Verlato, G, Torroni, L, Piessen, G, Pera, M & de Manzoni, G 2023, 'Clinical Features of Gastric Signet Ring Cell Cancer: Results from a Systematic Review and Meta-Analysis', Cancers, vol. 15, no. 21, 5191. https://doi.org/10.3390/cancers15215191

TY - JOUR

T1 - Clinical Features of Gastric Signet Ring Cell Cancer

T2 - Results from a Systematic Review and Meta-Analysis

AU - Dal Cero, Mariagiulia

AU - Bencivenga, Maria

AU - Liu, Drolaiz H.W.

AU - Sacco, Michele

AU - Alloggio, Mariella

AU - Kerckhoffs, Kelly G.P.

AU - Filippini, Federica

AU - Saragoni, Luca

AU - Iglesias, Mar

AU - Tomezzoli, Anna

AU - Carneiro, Fátima

AU - Grabsch, Heike I.

AU - Verlato, Giuseppe

AU - Torroni, Lorena

AU - Piessen, Guillaume

AU - Pera, Manuel

AU - de Manzoni, Giovanni

N1 - Funding Information: This work would not have been possible without the financial support of the “Fondazione Gianesini” and the “Ricerchiamo ONLUS”. H.I.G. is supported in part by the National Institute for Health and Care Research (NIHR) Leeds Biomedical Research Centre. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care. Publisher Copyright: © 2023 by the authors.

PY - 2023/11/1

Y1 - 2023/11/1

N2 - Background: Conflicting results about the prognostic relevance of signet ring cell histology in gastric cancer have been reported. We aimed to perform a meta-analysis focusing on the clinicopathological features and prognosis of this subgroup of cancer compared with other histologies. Methods: A systematic literature search in the PubMed database was conducted, including all publications up to 1 October 2021. A meta-analysis comparing the results of the studies was performed. Results: A total of 2062 studies referring to gastric cancer with signet ring cell histology were identified, of which 262 studies reported on its relationship with clinical information. Of these, 74 were suitable to be included in the meta-analysis. A slightly lower risk of developing nodal metastases in signet ring cell tumours compared to other histotypes was found (especially to undifferentiated/poorly differentiated/mucinous and mixed histotypes); the lower risk was more evident in early and slightly increased in advanced gastric cancer. Survival tended to be better in early stage signet ring cell cancer compared to other histotypes; no differences were shown in advanced stages, and survival was poorer in metastatic patients. In the subgroup analysis, survival in signet ring cell cancer was slightly worse compared to non-signet ring cell cancer and differentiated/well-to-moderately differentiated adenocarcinoma. Conclusions: Most of the conflicting results in signet ring cell gastric cancer literature could be derived from the lack of standardisation in their classification and the comparison with the different subtypes of gastric cancer. There is a critical need to strive for a standardised classification system for gastric cancer, fostering clarity and coherence in the forthcoming research and clinical applications.

AB - Background: Conflicting results about the prognostic relevance of signet ring cell histology in gastric cancer have been reported. We aimed to perform a meta-analysis focusing on the clinicopathological features and prognosis of this subgroup of cancer compared with other histologies. Methods: A systematic literature search in the PubMed database was conducted, including all publications up to 1 October 2021. A meta-analysis comparing the results of the studies was performed. Results: A total of 2062 studies referring to gastric cancer with signet ring cell histology were identified, of which 262 studies reported on its relationship with clinical information. Of these, 74 were suitable to be included in the meta-analysis. A slightly lower risk of developing nodal metastases in signet ring cell tumours compared to other histotypes was found (especially to undifferentiated/poorly differentiated/mucinous and mixed histotypes); the lower risk was more evident in early and slightly increased in advanced gastric cancer. Survival tended to be better in early stage signet ring cell cancer compared to other histotypes; no differences were shown in advanced stages, and survival was poorer in metastatic patients. In the subgroup analysis, survival in signet ring cell cancer was slightly worse compared to non-signet ring cell cancer and differentiated/well-to-moderately differentiated adenocarcinoma. Conclusions: Most of the conflicting results in signet ring cell gastric cancer literature could be derived from the lack of standardisation in their classification and the comparison with the different subtypes of gastric cancer. There is a critical need to strive for a standardised classification system for gastric cancer, fostering clarity and coherence in the forthcoming research and clinical applications.

KW - gastric cancer

KW - pathological classification

KW - poorly cohesive

KW - signet ring cells

KW - survival

U2 - 10.3390/cancers15215191

DO - 10.3390/cancers15215191

M3 - (Systematic) Review article

SN - 2072-6694

VL - 15

JO - Cancers

JF - Cancers

IS - 21

M1 - 5191

ER -